Equivalent Representation of Real and Illusory Contours in Macaque V4

The cortical processing of illusory contours provides a unique window for exploring the brain mechanisms underlying visual perception. Previous electrophysiological single-cell recordings demonstrate that a subgroup of cells in macaque V1 and V2 signal the presence of illusory contours, whereas recent human brain imaging studies reveal higher-order visual cortices playing a central role in illusory figure processing. It seems that the processing of illusory contours/figures may engage multiple cortical interactions between hierarchically organized processing stages in the ventral visual pathway of primates. However, it is not yet known in which brain areas illusory contours are represented in the same manner as real contours at both the population and single-cell levels. Here, by combining intrinsic optical imaging in anesthetized rhesus macaques with single-cell recordings in awake ones, we found a complete overlap of orientation domains in visual cortical area V4 for processing real and illusory contours. In contrast, the orientation domains mapped in early visual areas V1 and V2 mainly encoded the local physical stimulus features inducing the subjective perception of global illusory contours. Our results indicate that real and illusory contours are encoded equivalently by the same functional domains in V4, suggesting that V4 is a key cortical locus for integration of local features into global contours.

[1]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[2]  R. Gregory,et al.  Cognitive Contours , 1972, Nature.

[3]  R. Tennant,et al.  Inhibition of leukaemia virus replication by polyadenylic acid. , 1972, Nature: New biology.

[4]  G. Kanizsa Subjective contours. , 1976, Scientific American.

[5]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[6]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[7]  S. Grossberg,et al.  Neural dynamics of form perception: boundary completion, illusory figures, and neon color spreading. , 1985 .

[8]  D. Pollen,et al.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. , 1985, The Journal of physiology.

[9]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[10]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

[11]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[12]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[13]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[14]  Guy A. Orban,et al.  Illusory contour orientation discrimination , 1987, Vision Research.

[15]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  K. Nakayama,et al.  Subjective contours, tilt aftereffects, and visual cortical organization , 1989, Vision Research.

[20]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[21]  P. H. Schiller,et al.  The role of the primate extrastriate area V4 in vision. , 1991, Science.

[22]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[23]  G. Blasdel,et al.  Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Leslie G. Ungerleider,et al.  The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Michael J. Hawken,et al.  Macaque VI neurons can signal ‘illusory’ contours , 1993, Nature.

[26]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[27]  G. Orban,et al.  Cue-invariant shape selectivity of macaque inferior temporal neurons. , 1993, Science.

[28]  V. Ramachandran,et al.  On the perception of illusory contours , 1994, Vision Research.

[29]  Jon Driver,et al.  Parallel detection of Kanizsa subjective figures in the human visual system , 1994, Nature.

[30]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[31]  J. B. Levitt,et al.  Receptive fields and functional architecture of macaque V2. , 1994, Journal of neurophysiology.

[32]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[33]  L. Spillmann,et al.  Phenomena of Illusory Form: Can We Bridge the Gap between Levels of Explanation? , 1995, Perception.

[34]  W. Merigan,et al.  Basic visual capacities and shape discrimination after lesions of extrastriate area V4 in macaques , 1996, Visual Neuroscience.

[35]  Michael Bach,et al.  The abutting grating illusion , 1996, Vision Research.

[36]  K. Nakayama,et al.  Enhanced Perception of Illusory Contours in the Lower Versus Upper Visual Hemifields , 1996, Science.

[37]  R. Shapley,et al.  Spatial and Temporal Properties of Illusory Contours and Amodal Boundary Completion , 1996, Vision Research.

[38]  Leslie G. Ungerleider,et al.  Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques , 1996, Visual Neuroscience.

[39]  M. Sur,et al.  Orientation Maps of Subjective Contours in Visual Cortex , 1996, Science.

[40]  G. Ghose,et al.  Form processing modules in primate area V4. , 1997, Journal of neurophysiology.

[41]  D J Felleman,et al.  Modular Organization of Occipito-Temporal Pathways: Cortical Connections between Visual Area 4 and Visual Area 2 and Posterior Inferotemporal Ventral Area in Macaque Monkeys , 1997, The Journal of Neuroscience.

[42]  G Westheimer,et al.  Classifying illusory contours: edges defined by "pacman" and monocular tokens. , 1997, Journal of neurophysiology.

[43]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[44]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[45]  Nicholas V. Swindale,et al.  Orientation tuning curves: empirical description and estimation of parameters , 1998, Biological Cybernetics.

[46]  D J Felleman,et al.  Segregation and convergence of functionally defined V2 thin stripe and interstripe compartment projections to area V4 of macaques. , 1999, Cerebral cortex.

[47]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[48]  Geoffrey M. Ghose,et al.  Specialized Representations in Visual Cortex A Role for Binding? , 1999, Neuron.

[49]  S L Macknik,et al.  Optical images of visible and invisible percepts in the primary visual cortex of primates. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[50]  L. Spillmann From Elements to Perception: Local and Global Processing in Visual Neurons , 1999, Perception.

[51]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[52]  B. Gulyás,et al.  Neuronal correlates of real and illusory contour perception: functional anatomy with PET , 1999, The European journal of neuroscience.

[53]  G. Orban,et al.  Processing of kinetically defined boundaries in areas V1 and V2 of the macaque monkey. , 2000, Journal of neurophysiology.

[54]  W. Merigan Cortical area V4 is critical for certain texture discriminations, but this effect is not dependent on attention , 2000, Visual Neuroscience.

[55]  E. Peterhans,et al.  Anatomy and physiology of a neural mechanism defining depth order and contrast polarity at illusory contours , 2000, The European journal of neuroscience.

[56]  C. Connor,et al.  Shape representation in area V4: position-specific tuning for boundary conformation. , 2001, Journal of neurophysiology.

[57]  T. S. Lee,et al.  Dynamics of subjective contour formation in the early visual cortex. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  G. Blasdel,et al.  Functional Retinotopy of Monkey Visual Cortex , 2001, The Journal of Neuroscience.

[59]  C. Hung,et al.  Real and illusory contour processing in area V1 of the primate: a cortical balancing act. , 2001, Cerebral cortex.

[60]  D. Eagleman Visual illusions and neurobiology , 2001, Nature Reviews Neuroscience.

[61]  C. Connor,et al.  Population coding of shape in area V4 , 2002, Nature Neuroscience.

[62]  Jean Bullier,et al.  Shape discrimination deficits during reversible deactivation of area V4 in the macaque monkey. , 2002, Cerebral cortex.

[63]  A. Nieder,et al.  Seeing more than meets the eye: processing of illusory contours in animals , 2002, Journal of Comparative Physiology A.

[64]  John J. Foxe,et al.  The Spatiotemporal Dynamics of Illusory Contour Processing: Combined High-Density Electrical Mapping, Source Analysis, and Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[65]  D. Pollen,et al.  Spatial receptive field organization of macaque V4 neurons. , 2002, Cerebral cortex.

[66]  Tai Sing Lee,et al.  The Nature of Illusory Contour Computation , 2002, Neuron.

[67]  Ulf T Eysel,et al.  Illusions and Perceived Images in the Primate Brain , 2003, Science.

[68]  N. Rubin,et al.  fMRI Activation in Response to Illusory Contours and Salient Regions in the Human Lateral Occipital Complex , 2003, Neuron.

[69]  Eric Halgren,et al.  Cortical activation to illusory shapes as measured with magnetoencephalography , 2003, NeuroImage.

[70]  Tai Sing Lee,et al.  Hierarchical Bayesian inference in the visual cortex. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[71]  Jay Hegdé,et al.  How Selective Are V1 Cells for Pop-Out Stimuli? , 2003, The Journal of Neuroscience.

[72]  N. Logothetis,et al.  Integration of Local Features into Global Shapes Monkey and Human fMRI Studies , 2003, Neuron.

[73]  Leonard E. White,et al.  Mapping multiple features in the population response of visual cortex , 2003, Nature.

[74]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

[75]  M. Carandini,et al.  Mapping of stimulus energy in primary visual cortex. , 2005, Journal of neurophysiology.

[76]  Tanya I. Baker,et al.  Cortical maps of separable tuning properties predict population responses to complex visual stimuli. , 2005, Journal of neurophysiology.

[77]  Rufin Vogels,et al.  Processing of kinetic boundaries in macaque V4. , 2006, Journal of neurophysiology.

[78]  Eero P. Simoncelli,et al.  How MT cells analyze the motion of visual patterns , 2006, Nature Neuroscience.

[79]  J. Gallant,et al.  Spectral receptive field properties explain shape selectivity in area V4. , 2006, Journal of neurophysiology.

[80]  M. Seghier,et al.  Functional Neuroimaging Findings on the Human Perception of Illusory Contours , 2022 .

[81]  T. Poggio,et al.  A model of V4 shape selectivity and invariance. , 2007, Journal of neurophysiology.

[82]  G. Sáry,et al.  Illusory shape representation in the monkey inferior temporal cortex , 2007, The European journal of neuroscience.

[83]  Michael S. Landy,et al.  Orientation-Selective Adaptation to Illusory Contours in Human Visual Cortex , 2007, The Journal of Neuroscience.

[84]  C. Gilbert,et al.  Learning to Link Visual Contours , 2008, Neuron.

[85]  Ingo Schießl,et al.  Independent components of the haemodynamic response in intrinsic optical imaging , 2008, NeuroImage.

[86]  C. Baker,et al.  Critical spatial frequencies for illusory contour processing in early visual cortex. , 2008, Cerebral cortex.

[87]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[88]  G. Orban,et al.  Shape selectivity for camouflage-breaking dynamic stimuli in dorsal V4 neurons. , 2008, Cerebral cortex.

[89]  Ennio Mingolla,et al.  Multiple mechanisms of illusory contour perception. , 2008, Journal of vision.

[90]  Johan Wagemans,et al.  Modelling contrast discrimination data suggest both the pedestal effect and stochastic resonance to be caused by the same mechanism. , 2008, Journal of vision.

[91]  Ari Rosenberg,et al.  Models and measurements of functional maps in V1. , 2008, Journal of neurophysiology.

[92]  B. C. Motter Central V4 Receptive Fields Are Scaled by the V1 Cortical Magnification and Correspond to a Constant-Sized Sampling of the V1 Surface , 2009, The Journal of Neuroscience.

[93]  Tirin Moore,et al.  Influence and Limitations of Popout in the Selection of Salient Visual Stimuli by Area V4 Neurons , 2009, The Journal of Neuroscience.

[94]  E. Callaway,et al.  Parallel processing strategies of the primate visual system , 2009, Nature Reviews Neuroscience.

[95]  Nicole C. Rust,et al.  Selectivity and Tolerance (“Invariance”) Both Increase as Visual Information Propagates from Cortical Area V4 to IT , 2010, The Journal of Neuroscience.

[96]  Philip J. Kellman,et al.  A unified model of illusory and occluded contour interpolation , 2010, Vision Research.

[97]  Gregory Francis,et al.  Properties of Long-Range Illusory Contours Produced by Offset-Arcs , 2010, Perception.

[98]  A. Roe,et al.  Functional organization for color and orientation in macaque V4 , 2010, Nature Neuroscience.

[99]  Taihei Ninomiya,et al.  Differential architecture of multisynaptic geniculo-cortical pathways to V4 and MT. , 2011, Cerebral cortex.

[100]  J. Anthony Movshon,et al.  Neuronal Responses to Texture-Defined Form in Macaque Visual Area V2 , 2011, The Journal of Neuroscience.

[101]  Anitha Pasupathy,et al.  Partial Occlusion Modulates Contour-Based Shape Encoding in Primate Area V4 , 2011, The Journal of Neuroscience.